Deletion of mouse Rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality

Molecular and Cellular Biology

Volumn 24, Issue 16, 2004, Pages 7235-7248

  Hopkins, Kevin M ^a   Auerbach, Wojtek ^c,d   Wang, Xiang Yuan ^b   Hande, M Prakash ^a,e   Hang, Haiying ^a   Wolgemuth, Debra J ^b   Joyner, Alexandra L ^c   Lieberman, Howard B ^a,b  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b New York Univ School of Medicine ^*  (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d REGENERON PHARMACEUTICALS INC   (United States)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYUREA; NOCODAZOLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA SYNTHESIS; EMBRYO DEATH; EMBRYO DEVELOPMENT; GAMMA RADIATION; GENE DELETION; GENE FUNCTION; GENE FUSION; GENETIC COMPLEMENTATION; GENETIC STABILITY; LETHAL MUTANT; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAD9 GENE; RADIATION RESPONSE; RADIOSENSITIVITY; SCHIZOSACCHAROMYCES POMBE; ULTRAVIOLET IRRADIATION;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMOSOME ABERRATIONS; DNA DAMAGE; EMBRYO; GENE DELETION; GENE EXPRESSION REGULATION; GENES, CDC; GENOMIC INSTABILITY; HUMANS; HYDROXYUREA; IN SITU NICK-END LABELING; MICE; MICE, KNOCKOUT; NUCLEIC ACID SYNTHESIS INHIBITORS; RADIATION, IONIZING; STEM CELLS; SURVIVAL RATE;

ANIMALIA; MAMMALIA; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 3543028030     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.16.7235-7248.2004     Document Type: Article

References (86)

1. Aladjem, M. I., B. T. Spike, L. W. Rodewald, T. J. Hope, M. Klemm, R. Jaenisch, and G. M. Wahl. 1998. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 8:145-155.
2. Al-Khodairy, F., and A. M. Carr. 1992. DNA repair mutants defining G2 checkpoint pathways in S. pombe. EMBO J. 15:1343-1350.
3. Al-Khodairy, F., E. Fotou, K. S. Sheldrick, D. J. Griffiths, A. R. Lehman, and A. M. Carr. 1994. Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast. Mol. Biol. Cell 5:147-160.
4. Auerbach, W., J. H. Dunmore, V. Fairchild-Huntress, Q. Fang, A. B. Auerbach, D. Huszar, and A. L. Joyner. 2000. Establishment and chimera analysis of 129/SvEv- and C57BL/6-derived mouse embryonic stem cell lines. Bio-Techniques 29:1024-1032.
5. Barlow, C., S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried, D. Tagle, and A. Wynshaw-Boris. 1996. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86:159-171.
6. Bartkova, J., J. Lukas, and J. Bartek. 1997. Aberrations of the G1- and G1/S-regulating genes in human cancer. Prog. Cell Cycle Res. 3:211-220.
7. Bermudez, V. P., L. A. Lindsey-Boltz, A. J. Cesare, Y. Maniwa, J. D. Griffith, J. Hurwitz, and A. Sancar. 2003. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc. Natl. Acad. Sci. USA 100:1633-1638.
8. Bessho, T., and A. Sancar. 2000. Human DNA damage checkpoint protein hRAD9 is a 3′ to 5′ exonuclease. J. Biol. Chem. 275:7451-7454.
9. Brown, E. J., and D. Baltimore. 2000. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14:397-402.
10. Chapman D. L., and D. J. Wolgemuth. 1994. Expression of proliferating cell nuclear antigen in the mouse germ line and surrounding somatic cells suggests both proliferation-dependent and -independent modes of function. Int. J. Dev. Biol. 38:491-497.
11. Chen, M. J., Y. T. Lin, H. B. Lieberman, G. Chen, and E. Y. Lee. 2001. ATM-dependent phosphorylation of human Rad9 is required for ionizing radiation-induced checkpoint activation. J. Biol. Chem. 276:16580-16586.
12. Conner, F., D. Bertwistle, P. J. Mee, G. M. Ross, S. Swift, E. Grigorieva, V. L. Tybulewicz, and A. Ashworth. 1997. Tumorigenesis and a DNA repair defect in mice with a truncating Brca1 mutation. Nat. Genet. 17:423-430.
13. de Klein, A., M. Muijtjens, R. van Os, Y. Verhoeven, B. Smit, A. M. Carr, A. R. Lehmann, and J. H. Hoeijmakers. 2000. Targeted disruption of the cell- cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479-482.
14. Deng, C., P. Zhang, J. W. Harper, S. J. Elledge, and P. Leder. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are devfective in G1 checkpoint control. Cell 82:675-684.
15. Dietrich, P., I. Dragatsis, S. Xuan, S. Zeitlin, and A. Efstradiadus. 2000. Conditional mutagenesis in mice with heat shock promoter-driven cre transgenes. Mamm. Genome 11:196-205.
16. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
17. Duyao, M. P., A. B. Auerbach, A. Ryan, F. Persichetti, G. T. Barnes, S. M. McNeil, P. Ge, J. P. Vonsattel, J. F. Gusella, A. L. Joyner, et al. 1995. Inactivation of the mouse Huntington's disease gene homolog Hdh. Science 269:407-410.
18. Dymecki, S. M. 1996. A modular set of Flp, FRT and lacZ fusion vectors for manipulating genes by site-specific recombination. Gene 171:197-201.
19. Ellison, V., and B. Stillman. 17 November 2003, posting date. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol. 1:E33. [Online.]
20. Elson, A., Y. Wang, C. J. Daugherty, C. C. Morton, F. Zhou, J. Campos-Torres, and P. Leder. 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93:13084-13089.
21. Fantes, P. A., E. Warbrick, D. A. Hughes, and S. A. MacNeill. 1991. New elements in the mitotic control of the fission yeast Schizosaccharomyces pombe. Cold Spring Harbor Symp. Quant. Biol. 56:605-611.
22. Ford, J. C., F. Al-Khodairy, E. Fotou, K. S. Sheldrick, D. J. Griffiths, and A. M. Carr. 1994. 14-3-3 protein homologs required for the DNA damage checkpoint in fission yeast. Science 365:533-535.
23. Fox, M. E., and G. R. Smith. 1998. Control of meiotic recombination in Schizosaccharomyces pombe. Prog. Nucleic Acid Res. Mol. Biol. 61:345-378.
24. + and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev. 12:2560-2573.
25. Gowen, L. C., B. L. Johnson, A. M. Latour, K. K. Sulik, and B. H. Koller. 1996. Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nat. Genet. 12:191-194.
26. Griffith, J. D, L. A. Lindsey-Boltz, and A. Sancar. 2002. Structures of the human Rad17-replication factor C and checkpoint Rad 9-1-1 complexes visualized by glycerol spray/low voltage microscopy. J. Biol. Chem. 277:15233-15236.
27. Hakem, R., J. L. de la Pompa, C. Sirard, R. Mo, M. Woo, A. Hakem, A. Wakeham, J. Potter, A. Reitmair, F. Billia, E. Firpo, C. C. Hui, J. Roberts, J. Rossant, and T. W. Mak. 1996. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85:1009-1023.
28. Han, L.-L., M. P. Keller, W. Navidi, P. F. Chance, and N. Arnheim. 2000. Unequal exchange at the Charcot-Marie-Tooth disease type 1A recombination hot-spot is not elevated above the average genome rate. Hum. Mol. Genet. 9:1881-1889.
29. Hang, H., and H. B. Lieberman. 2000. Physical interactions among human checkpoint control proteins HUS1p, RAD1p and RAD9p, and implications for the regulation of cell cycle progression. Genomics 65:24-33.
30. + checkpoint control gene. J. Cell. Physiol. 177:241-247.
31. + alter hydroxyurea resistance, radioresistance and checkpoint control. Nucleic Acids Res. 28:4340-4349.
32. Hanks, M., W. Wurst, L. Anson-Cartwright, A. B. Auerbach, and A. L. Joyner. 1995. Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science 269:679-682.
33. Hartwell, L. H., and M. B. Kastan. 1994. Cell cycle control and cancer. Science 266:1821-1828.
34. Hartwell, L. H., and T. A. Weinert. 1989. Checkpoints: controls that ensure the order of cell cycle events. Science 246:629-634.
35. Hirai, A., A. Cheung, G. Duncan, P.-M. Girard, A. J. Elia, A. Wakeham, H. Okada, T. Sarkissian, J. A. Wong, T. Sakai, E. de Stanchina, R. G. Bristow, T. Suda, S. W. Lowe, P. A. Jeggo, S. J. Elledge, and T. W. Mak. 2002. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (ATM)-dependent and an ATM-independent manner. Mol. Cell. Biol. 22:6521-6532.
36. Hirai, I., and H.-G. Wang. 2002. A role of the C-terminal region of human Rad9 (hRad9) in nuclear transport of the hRad9 checkpoint complex. J. Biol. Chem. 277:25722-25727.
37. Hopkins, K. M., X. Wang, A. Berlin, H. Hang, H. M. Thaker, and H. B. Lieberman. 2003. Expression of mammalian paralogues of HRAD9 and Mrad9 checkpoint control genes in normal and cancerous testicular tissue. Cancer Res. 63:5291-5298.
38. Jin, C., and J. C. Reed. 2002. Yeast and apoptosis. Nat. Rev. Mol. Cell. Biol. 3:453-459.
39. Joyner, A. L. 2000. Gene targeting: a practical approach, 2nd ed., p. 7-11. IRL Press, New York, N.Y.
40. Keegan, K. S., D. A. Holtzman, A. W. Plug, E. R. Christenson, E. E. Brainerd, G. Flaggs, N. J. Bentley, E. M. Taylor, M. S. Meyn, S. B. Moss, A. M. Carr, T. Ashley, and M. F. Hoekstra. 1996. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10:2423-2437.
41. Kobori, J. A., E. Strauss, K. Minard, and L. Hood. 1986. Molecular analysis of the hotspot of recombination in the murine major histocompatibility complex. Science 234:173-179.
42. Komatsu, K., K. M. Hopkins, H. B. Lieberman, and H.-G. Wang. 2000. Schizosaccharomyces pombe Rad9 contains a BH3-like region and interacts with the anti-apoptotic protein Bcl-2. FEBS Lett. 481:122-126.
43. Komatsu, K., T. Miyashita, H. Hang, K. M. Hopkins, W. Zheng, S. Cuddeback, M. Yamada, H. B. Lieberman, and H.-G. Wang. 2000. Human homologue of S. pombe Rad9 interacts with Bcl-2/Bcl-XL and promotes apoptosis. Nat. Cell Biol. 2:1-6.
44. Kostrub, C. F., K. Knudson, S. Subramani, and T. Enoch. 1998. Hus1p, a conserved fission yeast checkpoint protein, interacts with Rad1p and is phosphorylated in response to DNA damage. EMBO J. 17:2055-2066.
45. Li, B., S. Boast, K. de los Santos, I. Schieren, M. Quiroz, S. L. Teitelbaum, M. M. Tondravi, and S. P. Goff. 2000. Mice deficient in Abl are osteoporotic and have defects in osteoblast maturation. Nat. Genet. 24:304-308.
46. Lieberman, H. B. 1995. Extragenic suppressors of Schizosaccharomyces pombe rad9 mutations uncouple radioresistance and hydroxyurea sensitivity from cell cycle checkpoint control. Genetics 141:107-117.
47. + checkpoint control gene. Proc. Natl. Acad. Sci. USA 93:13890-13895.
48. Liu, C. Y., A. Flesken-Nikitin, S. Li, Y. Zeng, and W. H. Lee. 1996. Inactivation of the mouse Brca1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development. Genes Dev. 10:1835-1843.
49. 2/M DNA damage checkpoint. Genes Dev. 14:1448-1459.
50. Ludwig, T., D. L. Chapman, V. E. Papaioannou, and A. Efstratiadis. 1997. Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev. 11:1226-1241.
51. Maser, R. S., and R. A. DePinho. 2002. Connecting chromosomes, crisis and cancer. Science 297:565-569.
52. Matise, M. P., W. Auerbach, and A. L. Joyner. 2000. Production of targeted embryonic stem cell clones, p. 101-132. In A. L. Joyner (ed.), Gene targeting. A practical approach, 2nd ed. Oxford University Press, New York, N.Y.
53. Matsuoka, S., M. Huang, and S. J. Elledge. 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282:1893-1897.
54. Nabetani, A., O. Yokoyama, and F. Ishikawa. 2004. Localization of hRad9, hHus1, hRad1 and hRad17, and caffeine-sensitive DNA replication at ALT (alternative lengthening of telomeres)-associated promyelocytic leukemia body. J. Biol. Chem. 279:25849-25857.
55. Nagy, A., and J. Rossant. 2000. Production and analysis of ES cell aggregation chimeras, p. 177-206. In A. L. Joyner (ed.), Gene targeting. A practical approach, 2nd ed. Oxford University Press, New York, N.Y.
56. Nakamura, T. M., B. A. Moser, and P. Russell. 2002. Telomere binding of checkpoint sensor and DNA repair proteins contributes to maintenance of functional fission yeast telomeres. Genetics 161:1437-1452.
57. Nyberg, K. A., R. J. Michelson, C. W. Putman, and T. A. Weinert. 2002. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36:617-656.
58. Page, A. W., and T. L. Orr-Weaver. 1997. Stopping and starting the meiotic cell cycle. Curr. Opin. Genet. Dev. 7:23-31.
59. Painter, R. B. 1981. Screening of mutagens by inhibition of DNA synthesis, p. 569-574. In E. C. Friedberg and P. C. Hanawalt (ed.), DNA repair. A laboratory manual of research procedures, vol. 1, part B. Marcel Dekker, Inc., New York, N.Y.
60. Papaioannou, V., and R. Johnson. 2000. Production of chimeras by blastocyst and morula injection of targeted ES cells, p. 133-175. In A. L. Joyner (ed.), Gene targeting. A practical approach, 2nd ed. Oxford University Press, New York, N.Y.
61. + checkpoint gene encodes an exonuclease. J. Biol. Chem. 273:18332-18339.
62. + checkpoint gene. J. Biol. Chem. 273:18340-18346.
63. Rattray, A, J., and L. S. Symington. 1993. Stimulation of meiotic recombination in yeast by an ARS element. Genetics 134:175-188.
64. Rauen, M., M. A. Burtelow, V. M. Dufault, and L. M. Karnitz. 2000. The human checkpoint protein hRad17 interacts with the PCNA-like proteins hRad1, hHus1, and hRad9. J. Biol. Chem. 275:29767-29771.
65. Rowley, R., S. Subramani, and P. G. Young. 1992. Checkpoint controls in Schizosaccharomyces pombe: rad1. EMBO J. 11:1335-1342.
66. Roos-Mattjus, P., K. M. Hopkins, A. J. Oestreich, B. T. Vroman, K. L. Johnson, S. Naylor, H. B. Lieberman, and L. M. Karnitz. 2003. Phosphorylation of human Rad9 is required for genotoxin-activated checkpoint signaling. J. Biol. Chem. 278:24428-24437.
67. Sanchez, Y., C. Wong, R. S. Thomas, R. Richman, Z. Wu, H. Piwnica-Wonns, and S. J. Elledge. 1997. Conservation of the Chk1 pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277:1497-1501.
68. Schmidt-Kastner, P. K., K. Jardine, M. Cormier, and M. W. McBurney. 1998. Absence of p53-dependent cell cycle regulation in pluripotent mouse cell lines. Oncogene 16:3003-3011.
69. St. Onge, R. P., B. D. Besley, M. Park, R. Casselman, and S. Davey. 2001. DNA damage-dependent and -independent phosphorylation of the hRad9 checkpoint protein. J. Biol. Chem. 276:41898-41905.
70. St. Onge, R. P., C. M. Udell, R. Casselman, and S. Davey. 1999. The human G2 checkpoint control protein RAD9 is a nuclear phosphoprotein that forms complexes with RAD1 and HUS1. Mol. Biol. Cell 10:1985-1995.
71. Strasser, A., L. O'Connor, and V. M. Dixit. 2000. Apoptosis signaling. Annu. Rev. Biochem. 69:217-245.
72. -/- mice. Genes Dev. 14:1439-1447.
73. Udell, C. M., S. K. Lee, and S. Davey. 1998. HRAD1 and MRAD1 encode mammalian homologues of the fission yeast rad1+ cell cycle checkpoint control gene. Nucleic Acids Res. 26:3971-3978.
74. Uematsu, Y., H. Kiefer, R. Schults, K. Fischer-Lindahl, and M. Steinmetz. 1986. Molecular characterization of a meitoic recombinational hotspot enhancing homologous equal crossing-over. EMBO J. 5:2123-2129.
75. Venclovas, C., and M. P. Thelen. 2000. Structure-based predictions of Rad1, Hus1 and Rad17 participation in sliding clamp and clamp loading complexes. Nucleic Acids Res. 28:2481-2493.
76. Volkmer, E., and L. M. Karnitz. 1999. Human homologues of Schizosaccharomyces pombe Rad1, Hus1 and Rad9 form a DNA damage-responsive protein complex. J. Biol. Chem. 274:567-570.
77. Walworth, N., S. Davey, and D. Beach. 1993. Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2. Nature 363:368-371.
78. Wang, L., C. L. Hsu, J. Ni, P. H. Wang, S. Yeh, P. Keng, and C. Chang. 2004. Human checkpoint protein hRad9 functions as a negative coregulator to repress androgen receptor transactivation in prostate cancer cells. Mol. Cell. Biol. 24:2202-2213.
79. Weiss, R. S., T. Enoch, and P. Leder. 2000. Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev. 14:1886-1898.
80. Xu, Y., T. Ashley, E. E. Brainerd, R. T. Bronson, M. S. Meyn, and D. Baltimore. 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10:2411-2422.
81. Yap, W. Y., and K. N. Kreuzer. 1991. Recombination hotspots in bacteriophage T4 are dependent on replication origins. Proc. Natl. Acad. Sci. USA 88:6043-6047.
82. Yin, Y., A. Zhu, Y. J. Jin, Y.-X. Liu, X. Zhang, K. M. Hopkins, and H. B. Lieberman. Human RAD9 checkpoint control/pro-apoptotic protein can activate transcription of p21. Proc. Natl. Acad. Sci. USA, 2004. 101:8864-8869
83. Yoshida, K., K. Komatsu, H.-G. Wang, and D. Kufe. 2002. c-Abl tyrosine kinase regulates the human Rad9 checkpoint protein in response to DNA damage. Mol. Cell. Biol. 22:3292-3300.
84. Yoshida, K., H.-G. Wang, Y. Miki, and D. Kufe. 2003. Protein kinase Cdelta is responsible for constitutive and DNA damage-induced phosphorylation of Rad9. EMBO J. 22:1431-1441.
85. Zhao, Y., and H. B. Lieberman. 1995. Schizosaccharomyces pombe: a model for molecular studies of eukaryotic genes. DNA Cell Biol. 5:359-371.
86. Zou, L., D. Cortez, and S. J. Elledge. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16:198-208.